Maize Carbohydrate Partitioning Defective33 Encodes an MCTP Protein and Functions in Sucrose Export from Leaves

Abstract

To sustain plant growth, development, and crop yield, sucrose must be transported from leaves to distant parts of the plant, such as seeds and roots. To identify genes that regulate sucrose accumulation and transport in maize (Zea mays), we isolated carbohydrate partitioning defective33 (cpd33), a recessive mutant that accumulated excess starch and soluble sugars in mature leaves. The cpd33 mutants also exhibited chlorosis in the leaf blades, greatly diminished plant growth, and reduced fertility. Cpd33 encodes a protein containing multiple C2 domains and transmembrane regions. Subcellular localization experiments showed the CPD33 protein localized to plasmodesmata (PD), the plasma membrane, and the endoplasmic reticulum. We also found that a loss-of-function mutant of the CPD33 homolog in Arabidopsis, QUIRKY, had a similar carbohydrate hyperaccumulation phenotype. Radioactively labeled sucrose transport assays showed that sucrose export was significantly lower in cpd33 mutant leaves relative to wild-type leaves. However, PD transport in the adaxial-abaxial direction was unaffected in cpd33 mutant leaves. Intriguingly, transmission electron microscopy revealed fewer PD at the companion cell-sieve element interface in mutant phloem tissue, providing a possible explanation for the reduced sucrose export in mutant leaves. Collectively, our results suggest that CPD33 functions to promote symplastic transport into sieve elements.

Genome-wide identification and characterization of multiple C2 domains and transmembrane region proteins in Gossypium hirsutum

“…In maize, ZmCpd33, a homolog of Arabidopsis QKY, promoted symplastic sucrose export from companion cells into sieve elements. The cpd33 mutants exhibited fewer PD at the companion cell-sieve element interface and excessive carbohydrate accumulation in the leaves [32]. These studies suggest that MCTPs are involved in diverse cellular processes mainly through intercellular or intracellular transport of other regulators.…”

“…Multiple C2 domains and transmembrane region proteins (MCTPs) contain three to four C2 domains in the N terminus and one to four transmembrane regions in the C terminus. MCTPs are evolutionary conserved proteins and have been identified in both animals and plants [7,21,24,25,[27][28][29][30][31][32]38]. Compared with animals and lower plants, higher plants contain significantly increased number of MCTPs, implying more diverse and specific functions of MCTPs in plant growth and development [7].…”

Genome-wide identification and characterization of multiple C2 domains and transmembrane region proteins in Gossypium hirsutum

“…Multiple C2 domains and transmembrane region proteins (MCTPs) contain three to four C2 domains in the N terminus and one to four transmembrane regions in the C terminus. MCTPs are evolutionary conserved proteins and have been identi ed in both animals and plants [7,21,24,25,[27][28][29][30][31][32]38]. Compared with animals and lower plants, higher plants contain signi cantly increased number of MCTPs, implying more diverse and speci c functions of MCTPs in plant growth and development [7].…”

“…The signi cantly increased number of MCTPs in higher plants may meet the requirement for more diverse and speci c functions of MCTPs in regulating various cellular processes in plants [7]. Functional analyses of MCTPs in various plant species demonstrated that MCTPs were involved in promoting owering, regulating shoot meristem development, controlling anther dehiscence, regulating cell growth anisotropy and exporting sucrose into sieve elements [7,24,25,[27][28][29][30][31][32]. GUS and GFP reporter assays of 16 AtMCTPs revealed that even MCTPs with close evolutionary relationship might be expressed in different tissues and some MCTPs might perform redundant or additive functions in certain tissues [7].…”

“…In maize, ZmCpd33, a homolog of Arabidopsis QKY, promoted symplastic sucrose export from companion cells into sieve elements. The cpd33 mutants exhibited fewer PD at the companion cell-sieve element interface and excessive carbohydrate accumulation in the leaves [32].…”